Docosahexaenoic acid-rich fish oil modulates the cerebral hemodynamic response to cognitive tasks in healthy young adults

Biological Psychology

Volumn 89, Issue 1, 2012, Pages 183-190

  Jackson, Philippa A ^a   Reay, Jonathon L ^a   Scholey, Andrew B ^b   Kennedy, David O ^a  

^a NORTHUMBRIA UNIVERSITY   (United Kingdom)

^b SWINBURNE UNIVERSITY OF TECHNOLOGY   (Australia)

Author keywords

Cognitive function; Docosahexaenoic acid; Healthy adults; Near infrared spectroscopy

Indexed keywords

DEOXYHEMOGLOBIN; DOCOSAHEXAENOIC ACID; FISH OIL; OLIVE OIL; OMEGA 3 FATTY ACID; OXYHEMOGLOBIN;

ADULT; ARTICLE; BLOOD LEVEL; BRAIN BLOOD FLOW; BRAIN FUNCTION; COGNITION; CONTROLLED STUDY; DIET SUPPLEMENTATION; EXECUTIVE FUNCTION; FEMALE; FOOD COMPOSITION; HEMATOLOGICAL PARAMETERS; HEMOGLOBIN BLOOD LEVEL; HUMAN; HUMAN EXPERIMENT; MALE; NEAR INFRARED SPECTROSCOPY; NORMAL HUMAN; OXYHEMOGLOBIN BLOOD LEVEL; PREFRONTAL CORTEX; PRIORITY JOURNAL; PSYCHOMOTOR PERFORMANCE; RESPONSE TIME; SPATIAL MEMORY; STROOP TEST; TASK PERFORMANCE; VOLUNTEER; WORKING MEMORY;

ADOLESCENT; ADULT; ANALYSIS OF VARIANCE; CEREBRAL CORTEX; CEREBROVASCULAR CIRCULATION; CHOICE BEHAVIOR; COGNITION; DIETARY SUPPLEMENTS; DOCOSAHEXAENOIC ACIDS; DOUBLE-BLIND METHOD; EXECUTIVE FUNCTION; FEMALE; FISH OILS; HEMODYNAMICS; HEMOGLOBINS; HUMANS; INHIBITION (PSYCHOLOGY); MALE; MEMORY, SHORT-TERM; NEUROPSYCHOLOGICAL TESTS; OXYHEMOGLOBINS; REACTION TIME; SPACE PERCEPTION; SPECTROSCOPY, NEAR-INFRARED; YOUNG ADULT;

EID: 84155164005     PISSN: 03010511     EISSN: 18736246     Source Type: Journal    
DOI: 10.1016/j.biopsycho.2011.10.006     Document Type: Article

References (77)

1. Aberg M.A., Aberg N., Brisman J., Sundberg R., Winkvist A., Toren K. Fish intake of Swedish male adolescents is a predictor of cognitive performance. Acta Paediatrica 2009, 98(3):555-560.
2. Antypa N., Van der Does A.J.W., Smelt A.H.M., Rogers R.D. Omega-3 fatty acids (fish-oil) and depression-related cognition in healthy volunteers. Journal of Psychopharmacology 2009, 23(7):831-840.
3. Appleton K.M., Rogers P.J., Ness A.R. Is there a role for n-3 long-chain polyunsaturated fatty acids in the regulation of mood and behaviour? A review of the evidence to date from epidemiological studies, clinical studies and intervention trials. Nutrition Research Reviews 2008, 21(1):13-41.
4. Awh E., Jonides J., Smith E.E., Schumacher E.H., Koeppe R.A., Katz S. Dissociation of storage and rehearsal in verbal working memory: evidence from positron emission tomography. Psychological Science 1996, 7(1):25-31.
5. Bertsch K., Hagemann D., Hermes M., Walter C., Khan R., Naumann E. Resting cerebral blood flow, attention, and aging. Brain Research 2009, 1267:77-88.
6. Bonoczk P., Panczel G., Nagy Z. Vinpocetine increases cerebral blood flow and oxygenation in stroke patients: a near-infrared spectroscopy and transcranial Doppler study. European Journal of Ultrasound 2002, 15(1-2):85-91.
7. Bourre J.M. Omega-3 fatty acids in psychiatry. Medical Science (Paris) 2005, 21(2):216-221.
8. Chance B., Leigh J.S., Miyake H., Smith D.S., Nioka S., Greenfeld R., et al. Comparison of time-resolved and time-unresolved measurements of deoxyhemoglobin in brain. Proceedings of the National Academy of Science of the United States America 1988, 85(14):4971-4975.
9. Dalton A., Wolmarans P., Witthuhn R.C., van Stuijvenberg M.E., Swanevelder S.A., Smuts C.M. A randomised control trial in schoolchildren showed improvement in cognitive function after consuming a bread spread, containing fish flour from a marine source. Prostaglandins Leukot Essent Fatty Acids 2009, 80(2-3):143-149.
10. Dangour A.D., Allen E., Elbourne D., Fasey N., Fletcher A.E., Hardy P., et al. Effect of 2-y n-3 long-chain polyunsaturated fatty acid supplementation on cognitive function in older people: a randomized, double-blind, controlled trial. American Journal of Clinical Nutrition 2010, 91(6):1725-1732.
11. De Caterina R., Basta G. n-3 fatty acids and the inflammatory response-biological background. European Heart Journal Supplements 2001, 3(D):D42-D49.
12. Drummond S.P.A., Brown G.G., Stricker J.L., Buxton R.B., Wong E.C., Gillin J.C. Sleep deprivation-induced reduction in cortical functional response to serial subtraction. Neuroreport 1999, 10(18):3745-3748.
13. Dullemeijer C., Durga J., Brouwer I.A., van de Rest O.V., Kok F.J., Brummer R.J.M., et al. n-3 Fatty acid proportions in plasma and cognitive performance in older adults. American Journal of Clinical Nutrition 2007, 86(5):1479-1485.
14. Engelhart M.J., Geerlings M.I., Ruitenberg A., Van Swieten J.C., Hofman A., Witteman J.C., et al. Diet and risk of dementia: does fat matter?: the Rotterdam study. Neurology 2002, 59(12):1915-1921.
15. Engstrom K., Saldeen A.S., Yang B., Mehta J.L., Saldeen T. Effect of fish oils containing different amounts of EPA, DHA, and antioxidants on plasma and brain fatty acids and brain nitric oxide synthase activity in rats. Upsala Journal of Medical Sciences 2009, 114(4):206-213.
16. Fallgatter A.J., Strik W.K. Right frontal activation during the continuous performance test assessed with near-infrared spectroscopy in healthy subjects. Neuroscience Letters 1997, 223(2):89-92.
17. Fallgatter A.J., Strik W.K. Frontal brain activation during the Wisconsin Card Sorting Test assessed with two-channel near-infrared spectroscopy. European Archives of Psychiatry and Clinical Neuroscience 1998, 248(5):245-249.
18. Farkas E., de Wilde M.C., Kiliaan A.J., Luiten P.G.M. Chronic cerebral hypoperfusion-related neuropathologic changes and compromised cognitive status: window of treatment. Drugs of Today 2002, 38(5):365-376.
19. Fedorova I., Salem N. Omega-3 fatty acids and rodent behavior. Prostaglandins Leukot Essent Fatty Acids 2006, 75(4-5):271-289.
20. Fitzgerald P.B., Srithiran A., Benitez J., Daskalakis Z.Z., Oxley T.J., Kulkarni J., et al. An fMRI study of prefrontal brain activation during multiple tasks in patients with major depressive disorder. Human Brain Mapping 2008, 29(4):490-501.
21. Fontani G., Corradeschi A., Felici F., Alfatti S., Migliori S., Lodi L. Cognitive and physiological effects of omega-3 polyunsaturated fatty acid supplementation in healthy subjects. European Journal of Clinical Investigation 2005, 35:691-699.
22. Fotuhi M., Mohassel P., Yaffe K. Fish consumption, long-chain omega-3 fatty acids and risk of cognitive decline or Alzheimer disease: a complex association. Nature Clinical Practice Neurology 2009, 5(3):140-152.
23. Freeman M.P., Hibbeln J.R., Wisner K.L., Davis J.M., Mischoulon D., Peet M., et al. Omega-3 fatty acids: evidence basis for treatment and future research in psychiatry. Journal of Clinical Psychiatry 2006, 67(12):1954-1967.
24. Hashimoto M., Hossain M.S., Yamasaki H., Yazawa K., Masumura S. Effects of eicosapentaenoic acid and docosahexaenoic acid on plasma membrane fluidity of aortic endothelial cells. Lipids 1999, 34(12):1297-1304.
25. Helland I.B., Smith L., Saarem K., Saugstad O.D., Drevon C.A. Maternal supplementation with very-long-chain n-3 fatty acids during pregnancy and lactation augments children's IQ at 4 years of age. Pediatrics 2003, 111(1):e39-e44.
26. Heude B., Ducimetiere P., Berr C. Cognitive decline and fatty acid composition of erythrocyte membranes-the EVA study. American Journal of Clinical Nutrition 2003, 77(4):803-808.
27. Hibbeln J.R., Davis J.M., Steer C., Emmett P., Rogers I., Williams C., et al. Maternal seafood consumption in pregnancy and neurodevelopmental outcomes in childhood (ALSPAC study): an observational cohort study. Lancet 2007, 369(9561):578-585.
28. Horrocks L.A., Farooqui A.A. Docosahexaenoic acid in the diet: its importance in maintenance and restoration of neural membrane function. Prostaglandins Leukot Essent Fatty Acids 2004, 70(4):361-372.
29. Hoshi Y. Functional near-infrared spectroscopy: current status and future prospects. Journal of Biomedical Optics 2007, 12(6).
30. Hoshi Y., Kobayashi N., Tamura M. Interpretation of near-infrared spectroscopy signals: a study with a newly developed perfused rat brain model. Journal of Applied Physiology 2001, 90(5):1657-1662.
31. Huppert T.J., Hoge R.D., Diamond S.G., Franceschini M.A., Boas D.A. A temporal comparison of BOLD, ASL, and NIRS hemodynamic responses to motor stimuli in adult humans. Neuroimage 2006, 29(2):368-382.
32. Innis S.M. Dietary (n-3) fatty acids and brain development. Journal of Nutrition 2007, 137(4):855-859.
33. Jackson, P.A., Deary, M., Reay, J.L., Scholey, A.B., Kennedy, D.O., 2011. Twelve weeks' dietary supplementation with 1g fish oil does not improve cognitive performance or mood in healthy young adults. British Journal of Nutrition. doi:10.1017/S00071141100403X.
34. Jasdzewski G., Strangman G., Wagner J., Kwong K.K., Poldrack R.A., Boas D.A. Differences in the hemodynamic response to event-related motor and visual paradigms as measured by near-infrared spectroscopy. Neuroimage 2003, 20(1):479-488.
35. Joy C.B., Mumby-Croft R., Joy L.A. Polyunsaturated fatty acid supplementation for schizophrenia. Cochrane Database of Systematic Reviews 2006, (3).
36. Kalmijn S., Feskens E.J., Launer L.J., Kromhout D. Polyunsaturated fatty acids, antioxidants, and cognitive function in very old men. American Journal of Epidemiology 1997, 145(1):33-41.
37. Kanamaru Y., Kikukawa A., Miyamoto Y., Hirafuji M. Dimenhydrinate effect on cerebral oxygen status and salivary chromogranin-A during cognitive tasks. Progress in neuropsychopharmacology & Biological Psychiatry 2008, 32(1):107-115.
38. Kennedy D.O., Haskell C.F. Haemodynamic and behavioural effects of caffeine in habitual and non-habitual consumers of caffeine: a near-infrared spectroscopy study. Biological Psychology 2011, 86(3):298-306.
39. Kennedy D.O., Jackson P.A., Elliott J.M., Scholey A.B., Robertson B.C., Greer J., et al. Cognitive and mood effects of 8 weeks' supplementation with 400mg or 1000mg of the omega-3 essential fatty acid docosahexaenoic acid (DHA) in healthy children aged 10-12 years. Nutritional Neuroscience 2009, 12(2):48-56.
40. Kennedy D.O., Wightman E.L., Reay J.L., Lietz G., Okello E.J., Wilde A., et al. Effects of resveratrol on cerebral blood flow variables and cognitive performance in humans: a double-blind, placebo-controlled, crossover investigation. American Journal of Clinical Nutrition 2010, 91(6):1590-1597.
41. Keppel G. Design and analysis 1991, Prentice Hall, Upper Saddle River, NJ, United States.
42. Kirby A., Woodward A., Jackson S., Wang Y., Crawford M.A. A double-blind, placebo-controlled study investigating the effects of omega-3 supplementation in children aged 8-10 years from a mainstream school population. Research in Developmental Disabilities 2010, 31(3):718-730.
43. Kitaura H., Uozumi N., Tohmi M., Yamazaki M., Sakimura K., Kudoh M., et al. Roles of nitric oxide as a vasodilator in neurovascular coupling of mouse somatosensory cortex. Neuroscience Research 2007, 59(2):160-171.
44. Lawrence N.S., Ross T.J., Stein E.A. Cognitive mechanisms of nicotine on visual attention. Neuron 2002, 36(3):539-548.
45. Li P., Kim S.W., Li X.L., Datta S., Pond W.G., Wu G.Y. Dietary supplementation with cholesterol and docosahexaenoic acid increases the activity of the arginine-nitric oxide pathway in tissues of young pigs. Nitric Oxide-Biology and Chemistry 2008, 19(3):259-265.
46. Lim W.S., Gammack J.K., Van Niekerk J., Dangour A.D. Omega 3 fatty acid for the prevention of dementia. Cochrane Database of Systematic Reviews 2006, (1).
47. Marx E., Deutschlander A., Stephan T., Dieterich M., Wiesmann M., Brandt T. Eyes open and eyes closed as rest conditions: impact on brain activation patterns. Neuroimage 2004, 21(4):1818-1824.
48. McNamara R.K., Carlson S.E. Role of omega-3 fatty acids in brain development and function: potential implications for the pathogenesis and prevention of psychopathology. Prostaglandins Leukot Essent Fatty Acids 2006, 75(4-5):329-349.
49. McNamara R.K., Able J., Jandacek R., Rider T., Tso P., Eliassen J.C., et al. Docosahexaenoic acid supplementation increases prefrontal cortex activation during sustained attention in healthy boys: a placebo-controlled, dose-ranging, functional magnetic resonance imaging study. American Journal of Clinical Nutrition 2010, 91(4):1060-1067.
50. Minami M., Kimura S., Endo T., Hamaue N., Hirafuji M., Togashi H., et al. Dietary docosahexaenoic acid increases cerebral acetylcholine levels and improves passive avoidance performance in stroke-prone spontaneously hypertensive rats. Pharmacology Biochemistry and Behavior 1997, 58(4):1123-1129.
51. Mori T.A., Woodman R.J. The independent effects of eicosapentaenoic acid and docosahexaenoic acid on cardiovascular risk factors in humans. Current Opinion in Clinical Nutrition and Metabolic Care 2006, 9(2):95-104.
52. Moriguchi T., Greiner R.S., Salem N. Behavioral deficits associated with dietary induction of decreased brain docosahexaenoic acid concentration. Journal of Neurochemistry 2000, 75(6):2563-2573.
53. Morris M.C., Evans D.A., Bienias J.L., Tangney C.C., Bennett D.A., Wilson R.S., et al. Consumption of fish and n-3 fatty acids and risk of incident Alzheimer disease. Archives of Neurology 2003, 60(7):940-946.
54. Obrig H., Villringer A. Beyond the visible-imaging the human brain with light. Journal of Cerebral Blood Flow and Metabolism 2003, 23(1):1-18.
55. Osendarp S.J.M., Baghurst K.I., Bryan J., Calvaresi E., Hughes D., Hussaini M., et al. Effect of a 12-mo micronutrient intervention on learning and memory in well-nourished and marginally nourished school-aged children: 2 parallel, randomized, placebo-controlled studies in Australia and Indonesia. American Journal of Clinical Nutrition 2007, 86(4):1082-1093.
56. Owen A.M., Evans A.C., Petrides M. Evidence for a two-stage model of spatial working memory processing within the lateral frontal cortex: a positron emission tomography study. Cerebral Cortex 1996, 6(1):31-38.
57. Parkes L.M., Rashid W., Chard D.T., Tofts P.S. Normal cerebral perfusion measurements using arterial spin labeling: reproducibility, stability, and age and gender effects. Magnetic Resonance in Medicine 2004, 51(4):736-743.
58. Richter M.M., Zierhut K.C., Dresler T., Plichta M.M., Ehlis A.C., Reiss K., et al. Changes in cortical blood oxygenation during arithmetical tasks measured by near-infrared spectroscopy. [Article]. Journal of Neural Transmission 2009, 116(3):267-273.
59. Rogers P.J., Appleton K.M., Kessler D., Peters T.J., Gunnell D., Hayward R.C., et al. No effect of n-3 long-chain polyunsaturated fatty acid (EPA and DHA) supplementation on depressed mood and cognitive function: a randomised controlled trial. British Journal of Nutrition 2008, 99(2):421-431.
60. Rosenthal J.M., Amiel S.A., Yaguez L., Bullmore E., Hopkins D., Evans M., et al. The effect of acute hypoglycemia on brain function and activation-a functional magnetic resonance imaging study. Diabetes 2001, 50(7):1618-1626.
61. Ryan A.S., Nelson E.B. Assessing the effect of docosahexaenoic acid on cognitive functions in healthy, preschool children: a randomized, placebo-controlled, double-blind study. Clinical Pediatrics (Philadelphia) 2008, 47(4):335-362.
62. Schecklmann M., Ehlis A.C., Plichta M.M., Fallgatter A.J. Functional near-infrared spectroscopy: a long-term reliable tool for measuring brain activity during verbal fluency. Neuroimage 2008, 43(1):147-155.
63. Schluter N.D., Krams M., Rushworth M.F.S., Passingham R.E. Cerebral dominance for action in the human brain: the selection of actions. Neuropsychologia 2001, 39(2):105-113.
64. Sorond F.A., Schnyer D.M., Serrador J.M., Milberg W.P., Lipsitz L.A. Cerebral blood flow regulation during cognitive tasks: effects of healthy aging. Cortex 2008, 44(2):179-184.
65. Steinbrink, J., Villringer, A., Kempf, F., Haux, D., Boden, S., Obrig, H., 2005. Illuminating the BOLD signal: combined fMRI-fNIRS studies. Paper presented at the International School on Magnetic Resonance and Brain Function, Erice, ITALY (May 23-29).
66. Stroop J.R. Studies of Interference in Serial Verbal Reactions. Journal of Experimental Psychology: General 1992, 121(1):15-23. (Reprinted from Journal Experimental-Psychology, vol. 18, 1935, pp. 643-662).
67. Sublette M.E., Milak M.S., Hibbeln J.R., Freed P.J., Oquendo M.A., Malone K.M., et al. Plasma polyunsaturated fatty acids and regional cerebral glucose metabolism in major depression. Prostaglandins Leukot Essent Fatty Acids 2009, 80(1):57-64.
68. Tamura M., Hoshi Y., Okada F. Localized near-infrared spectroscopy and functional optical imaging of brain activity. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 1997, 352(1354):737-742.
69. Tsukada H., Kakiuchi T., Ando I., Shizuno H., Nakanishi S., Ouchi Y. Regulation of cerebral blood flow response to somatosensory stimulation through the cholinergic system: a positron emission tomography study in unanesthetized monkeys. Brain Research 1997, 749(1):10-17.
70. Tsukada H., Kakiuchi T., Fukumoto D., Nishiyama S., Koga K. Docosahexaenoic acid (DHA) improves the age-related impairment of the coupling mechanism between neuronal activation and functional cerebral blood flow response: a PET study in conscious monkeys. Brain Research 2000, 862(1-2):180-186.
71. Tsukada H., Sato K., Kakiuchi T., Nishiyama S. Age-related impairment of coupling mechanism between neuronal activation and functional cerebral blood flow response was restored by cholinesterase inhibition: PET study with microdialysis in the awake monkey brain. Brain Research 2000, 857(1-2):158-164.
72. Turnbull T., Cullen-Drill M., Smaldone A. Efficacy of omega-3 fatty acid supplementation on improvement of bipolar symptoms: a systematic review. Archives of Psychiatric Nursing 2008, 22(5):305-311.
73. Uludag K., Dubowitz D.J., Yoder E.J., Restom K., Liu T.T., Buxton R.B. Coupling of cerebral blood flow and oxygen consumption during physiological activation and deactivation measured with fMRI. Neuroimage 2004, 23(1):148-155.
74. Van Breukelen G.J.P. ANCOVA versus change from baseline had more power in randomized studies and more bias in nonrandomized studies. Journal of Clinical Epidemiology 2006, 59(12):1334. (Correction).
75. Vanderhasselt M.A., De Raedt R., Baeken C. Dorsolateral prefrontal cortex and Stroop performance: tackling the lateralization. Psychonomic Bulletin and Review 2009, 16(3):609-612.
76. Villringer A., Dirnagl U. Coupling of brain activity and cerebral blood-flow-basis of functional neuroimaging. Cerebrovascular and Brain Metabolism Reviews 1995, 7(3):240-276.
77. Willis L.M., Shukitt-Hale B., Joseph J.A. Dietary polyunsaturated fatty acids improve cholinergic transmission in the aged brain. Genes and Nutrition 2009, 4(4):309-314.